Proprioceptors and their contribution to somatosensory mapping:

complex messages require complex processing'

PETERB. C. MATTHEWS
Laboratog?! ofPhy.~io!ogy,University of O.xf~rd~,
$/nil~ersl'Q Parks Road, 0xfi)rd 8 X d dPT, U . K
Received June 29, 1987

P. B . C. 1988. Proprioceptors and their contribution to somatosensory mapping: complex messages r e q u i ~

MATTHEWS,
complex processing . Can. J. Physiol. Pham~acol.66: 430-438.
This review of other people's work concentrates on two matters. First, which of the various receptors are chiefly involved in
creating the central representations or maps of the body that both underlie the conscious perception of our body image and are
needed to control our motor performance. Second, how are these relatively well-charted signals used in sensorimotor mapping,
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with particular attention paid 80 various human psychophysical observations and illusions that throw light on the central
integrative rnechanisrns involved. Detailed citation is largely restricted to developments since earlier reviews.

MATTHEWS.
P. B . C. 1988. Proprioceptors and their contribution to somatosensory mapping: complex messages require
complex processing. Can. J. Physical. P h m a c o l . 66 : 430-438.
Cette rkvision du travail d'autres chercheurs traite de deux 'sujets en particulier. Premikrement, des divers rkcepteurs
princhpalement impliquks dams la repdsentation centrale ou N mapping >> du c o p s et qui somt sous-jacents a la perception
consciente de notre image coporelle et nkcessaires au contr6le moteur. Beuxi&mement, de la rnanikre ddont ces signaux
relativement bien structurks sont utilisks dans la representation (mapping) scnsorirnotrice; on porte une attention particulikre aux
diverses observations physiologiques humaines et aux illusions qui aident a comprendre les mCcanismes iintkgratifs centraux
impliquCs. On rapporte en detail principalenaent les dkveloppements obtenus depuis Ies dernikres rCvisions.
Can. J. Physiol. Pharmacol. 1988.66:430-438.

(Traduit par la revue]

The old simplicity TABLE

1 . Receptors that transmit signals during movement
Thirty years ago things looked relatively simple. The joint Position sense Possible neural inputs
receptors were in, and everything else was out. Sksglund (1956,
1973) provided the classical picture of their behaviour. On the I)Joint In capsule
basis of his study on the cat knee, it came to be rather widely In ligaments
believed that joints possessed an array sf receptors, each with its
IE)Skin Fast adapting I and EI
own preferred angle of firing and active over only a limited part Slow adapting J and II
of the angular range of a joint. Thus the problem of constructing
a central map seemed to be the familiar one of requiring the 1EI)MuscHe Spindle: primary and secondary
Tendon organ
higher centres simply to recognize which receptors were active
and which were silent. How the body image was represented IV)Motor centres Corollary discharges
- -

was not at that stage a useful question, and people seem not to
have bothered about the difference between mapping the
position of a cutaneous stimulus on a pre-existing map of the
body surface, which can be thought of simply in terms of
receptive fields, and the problem of changing the relative
coordinates of the component parts of the map of the body image
as the body moves. Minor complications were recognized, such
as that the firing of the joint receptors was altered by contraction
of the nearby muscles, but this seems to have been a second
order effect introducing inaccuracy, perhaps, but not upsetting
the picture. This simplicity has now vanished; joint receptors
are largely out and muscle receptors are in9raising the question
as to how their signals can be read higher centres to
produce what is needed.
Receptors potentially contributing to position sense
Table 1 lists the numerous receptors that transmit signals
whenever we move. The question is which of them contribute
significantly to position sense, using this term in its widest and
loosest sense. I should note here that position sense can be
presumed to be concerned primarily with self-induced move-
'This paper was presented at eke IX International Symposium of
the Centre de recherche en sciences neurologiques, Universitk de
Montrkal, entitled Spatial Representations and Sensorimotor Trans-
fornations (Montrkal, Qud., May 28-29, 1987), and has undergone
the Journal's usual peer review.
Printed in Canada I Impfimt au Canada
ment and the disturbances the environment imposes upon us
while we are doing something. The standard neurological test of
"position sense,)' namely waggling the patient's passive finger,
does not comespond to any comnlonly occurring natural
stimulus. The detection of such essentially external stimuli
cannot be the prime function of the internally placed propriocep-
tors. A priori, this would seem to fall equally within the sphere
of action of the cutaneous receptors.
There is now a comprehensive classification of the large
cutaneous afferent receptors, but there is no point in dwelling on
the details. A recent shown by recording
from single fibres in man, is that for the hand virtually all of
these receptors are excited whenever we move it (Hulliger et al.
1979). Introspection tells us that the sensation during movement
bears no relation to that elicited by an external stimulus.
Although most of the s m e afferent receptors may be presumed
to be activated, the signals would seem to be handled differently
in the two cases, with those produced during movement being at
least partly denied access to the sensorium. As with the visual
suppression that occurs when we make a saccadic eye move-
ment, two sorts of mechanism could be responsible for the
gating. First, it could be the result of movement producing a
particular pattern of afferent activity, unlike that normally
produced by external stimuli, which then of itself triggers the
 reading system to behave in a particular way. Second, and with
classic physiological support, the afferent signal elicited by
movement may be operated upon in conjunction with some
component of the motor command which tells the analysing
centres (such as the dorsal column nuclei) that the sensory
signals are self-generated rather than externally generated. In
%pernay>tern the motor centres send a corollary discharge to the
sensory centres to allow them to interpret the sensory message
appropriately. These are included at the bottom of Table 1, as
there is no doubt on anatomical grounds that there are plenty of
internal connections available inside the GNS.
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Joint receptors
Joint afferent receptors have long been recognized histologi-
cally, lying both in the capsule and on any special ligaments.
The reason they are now out of favour is that single fibre
recordings in animals, especially those by Burgess and Clark
(1969) in the cat and by Grigg and Greenspan (1977) in the
monkey, show that for the knee they are only effectively excited
by moving the joint to one or other of its extremes. In the middle
of the range most if not all are normally quite silent, including
while the joint is being moved. If there is no afferent signal,
Can. J. Physiol. Pharmacol. 1988.66:430-438.
there can be no contribution to so-called "joint position sense"
and the body image. Fenell (B880),however, has been fighting
a rearguard action and believes that, though weak, the joint
afferent discharge is enough to help signal throughout the full
range of joint action; recent human experiments support his
view for the awareness of finger movement (Ferrell et al. 1987),
but even he does not claim that they are exclusively responsible,
as was the view generally held 20 years ago. Some of the smaller
knee-joint afferents have recently been found to be excited by
nonnoxious stimuli (Schaible and Schmidt 1983), but their
pattern of firing was such that, like the large afferents, they were
considered to be "mainly engaged in signalling that the joint is
about to leave its working range."
A few years ago it appeared as if the hip joint, with its
complex range of motion, was equipped with large joint
afferents firing throughout its range of movement. But on
reinvestigating the matter, Rossi and Grigg (1982) found that
these are muscle spindle afferents supplying the inferior
gernellus muscle and the joint receptors behave once again as
"limit detectors." For the cat elbow, however, Baxendale and
Fenell (1983) using multifibre recording have described an
appreciable level of midrange activity, which they adamantly
claim comes from joint rather than muscle afferents. It remains
an open question whether the contribution provided by joint
receptors varies from joint to joint. In addition, it should be
remembered that a given receptor will fire phasically during
joint movement over a wider range than it will fire tonically to
maintained displacement. They are thus somewhat better placed
to signal the occurrence of movement than to provide a
continuing measure of absolute position. By studying isolated
innervated sections of the joint capsule, Grigg and Hoffman
(1982) showed that the essential stimulus to the important and
numerous Ruffini receptors is stretch of the capsule rather than
transverse compression. This "explains" both why the receptors
are predominantly excited by movements to the extremes, for
only then does the capsule become taut, and why, as known
since Skoglund (1956), they may be excited on contraction of
nearby muscles, for this may help tense the capsule. In contrast,
the Golgi-Mazzoni receptors found on the inner surface of the
capsule are tuned to transverse pressure on the capsule (Grigg et
d.1982). They will only fire tonically on localized compression
of the capsule or on raising the intracapsular pressure by the
infusion of saline. However, they fire phasically in response to a
variety of less specific stimuli, including capsular stretch, and
so presumably respond during phasic muscle contractions. As
emphasized by Grigg and Greenspan (1973), the various
excitatory effects sf muscular contraction raise the possibility
that joint receptors may play a larger part in the signalling of
active movements than passive movements, including at inter-
mediate joint angles. These also greatly complicate the task of
"reading" the joint signal in terns of absolute position, since it is
not uniquely dependent on joint angle, but depends also upon
the behaviour of a variety of muscles. In conclusion, it seems
unlikely that joint receptors could be a regular source of
information for constructing the body image, but it would be
premature to dismiss them entirely, particularly in the signalling
of movement.
Muscle receptors
This brings us to the muscle receptors, and note that Table 1
neglects the free sensory endings supplied by the smallest nerve
fibres; these seem unlikely to be relevant in the present context.
The tendon organs lie in series with the muscle and have a low
enough threshold for some of them to respond whenever a
muscle contracts. Their sensory contribution would be expected
to be in the genesis of sensations of force and of effort rather
than of position, and even here corollary discharges seem to be
at least equally involved (Mceloskey 1978, 1981), so their
sensory role remains largely enigmatic. Of undoubted impsr-
tance for the present purposes are the muscle spindle afferents
that lie in parallel with the main muscle and so signal its length;
in addition they can be specifically excited by the fusimotor
system or gamma efferents.
It continues to merit emphasis that there are functionally
separable primary and secondary spindle afferents, differing in
their sensitivity to dynamic stimuli, so the muscle spindle is
providing two channels of information and is thus probably
capable of simultaneously signalling the values of two separate
mechanical parameters, perhaps length and velocity (Matthews
1972, 1981). Both types sf afferent fire more rapidly while a
muscle is k i n g stretched than when its length is held constant,
but the difference in firing is much greater for the primary
ending. Thus the primary ending is much more of a movement
detector, and the secondary more of a length detector. It will be
argued later that we have a sense of absolute position,
independent of awareness of movement. This could be based on
the firing of just the spindle secondary endings, for with
appropriate gamma bias their dynamic sensitivity may be very
small. In addition, we have a quantitatively graded sensation of
joint angular velocity, which is at least partly based on the
discharge of spindle primary afferents. It is important to note
that these do not give a pure velocity signal, but also fire
tonically with the muscle at a constant length; thus a single
observation on their firing frequency cannot tell us, or the
sensory centres, whether a joint is moving or still. It seems
possible, though this is by no means proven, that this difficulty
could be overcome, and angular velocity measured independent
of position, by combining the signals from primary and
secondary endings in an appropriate integrative centre. Know-
ledge of present position could also be based on a detailed
memory of past movement, as in the integrating accelerometers
used in navigation. However, the demands that this
 432 CAN. J . PWYSIOL. PHARMACOC. VOC. 66, 1988
the accuracy of instrumentation and computation remove much
of its biological appeal.
Evidence for spindle contribution
Vibration
With the dethronement of the joint receptors, the spindle
signals are now the ones believed to be chiefly responsible for
position sense and kinaesthesia. This was, of course, Sheuing-
ton's view at the turn of the century, but for a variety of reasons
it came to be discarded (see Matthews 1977, 1982). The initial
evidence for its reinstatement was derived from the use of
100 Hz vibration in human subjects, and this has continued to be
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an important tool. The value of vibration is that it provides a
particularly powerful stimulus for the spindle primary afferents.
Because of their high dynamic sensitivity they are tricked, so to
speak, into firing at a high frequency in a way they would
normally only do on being rapidly stretched.
The subjective effects of applying vibration to human
muscles and tendons were first analysed in detail by Goodwin,
McCloskey, and Matthews (1972) and are now well known.
The chief phenomenon is particularly well shown by vibrating
the biceps tendon of one a m while the blindfolded sub~ectis
Can. J. Physiol. Pharmacol. 1988.66:430-438.
told to keep his sther a m aligned with where he perceives the
vibrated a m to be. He then signals that the vibrated arm feels as
if it is more extended than it actually is; that is, as where it would
be if biceps were to be grossly stretched. The generally accepted
interpretation is that the vibration-induced afferent firing is
being treated as if it were due to muscle stretch, and is used to
update the body image; in other words spindle primary afferent
signals do contribute to position sense. Various points still merit
emphasis. First, note that the sensory information derived from
muscle does not lead to a sensation of something happening in
the muscle itself, but is refemed to the joint and used to indicate
its position. Second, as a logical corollary, it can be noted that
vibration of the antagonist, triceps, leads to the feeling that the
elbow is being flexed rather than extended. Thus the subjective
awareness sf joint position would seem to be derived from
summing, with appropriate signs, the spindle activity from all
the muscles acting at a given joint. Third, if one questions the
subject about what he is actually feeling and what he is
signalling with his refexnce m , he says that he is largely
following a sensation of movement of the vibrated arm, and that
it is rotating at constant velocity, rather than that it has simply
taken up a new constant position. But pointing tests suggest that
there is also a systematic distortion of a sense of absolute
position. The chief conclusion is that muscle afferents do
contribute to psition sense, as has since been amply supported
by other types of experiment.
Tendon pedlking
The most direct type of experiment has recently been repeated
by McCloskey et al. (1983) and by Moberg (19831, each of
whom independently called upon a surgical colleague to acutely
expose one sf their own tendons so that it could be pulled upon
in the laboratory. Ow pulling the tendon of McCloskey9s
extensor hallucis longus by 0.5 mrn or more in the direction
required to stretch the muscle, he reported the subjective
experience of his big toe being moved downwards, as to be
expected from the vibration experiments and in accordance with
the view that muscle afferents contribute to position sense.
Moberg, however, came to a very different conclusion on the
basis of having his finger flexor tendons pulled upon. First,
sensations of joint movement were very hard to elicit, pmticul-
a l y in relation to those evoked by pulling upon the tendons so as
to actually move the finger joints. Second, when muscle pulling
did produce a sensation of movement, he attributed it to
excitation of cutaneous receptors overlying the muscle rather
than of muscle receptors themselves .
This direct conflict over an experiment that few would wish to
repeat is most unfortunate; but in my view the balance of
evidence, including that of other workers, favours McCloskey
rather than Moberg and one can accept that the muscle afferent
discharge elicited on tendon pulling does lead to sensations of
movement of the appropriate joint. This view is fortified by the
more recent experiments of Gandevia (1985) with electrical
stimulation of the u l n a nerve at the wrist. By careful adjustment
of the stimulus strength and electrode position, he was able to
elicit sensations of finger movement without eliciting either any
overt muscular contraction or the cutaneous paraesthesiae
which axe so prominent on stimulation of a cutaneous nerve. It
seems likely that the sensations of movement were produced by
stimulating the Ia afferents from the spindle primary endings,
since the joint afferents are appreciably smaller and would not
be expected to be stimulated at below the motor threshold.
Relative contibutions of skin, joint, and muscle
Sense sf movement
On the basis of this and other evidence, virtually everybody
concerned now agrees that muscle afferents do contribute to
position sense. The precise extent to which joint and cutaneous
afferents also do so remains unresolved. For the knee, a variety
of experiments argue that neither provides a significant contri-
bution (Burgess et al. 1982). However, for the jnger the
experiments of Gandevia et al. (1983) show that one or both of
them contribute to the detection of passive imposed movements,
provided these are applied relatively rapidly. They studied the
perception sf a displacement applied at various velocities to the
terminal interphalangealjoint of the middle finger. They did this
with the finger in two different positions. When the finger is
extended, displacing the finger tip potentially excites A1 types of
afferent. The muscles change their length, joint receptors may
or may not be excited depending upon whether their midrange
silence is absolute, and some cutaneous receptors around the
flexure lines must be activated. When the middle finger is fully
flexed, while its neighbours are extended by external restraint, it
becomes impossible to move its teminal joint voluntarily; this
is because of the way the tendons of the muscles to the different
fingers are interconnected. Passive movement of the joint is then
no longer transmitted to the muscles, which have been function-
ally "'disengaged," so that the effects of an applied displacement
are confined to skin and joint. The contribution of muscles on
their own can be studied, with the finger extended, by
ring-blocking the finger and SO eliminating the skin and joint
afferents; the muscles, of course, lie safely out of the way of the
anaesthetic.
Using relatively rapid movements Gandevia et al. (1983)
found that displacements were most reliably detected when all
the peripheral inputs were operative, next best when the muscle
afferents were working on their own, and least well (and
especially badly at lower velocities) when only skin and joint
afferents were active. These two latter inputs could not then be
separated, but the recent work sf Ferrell et al. (198'7) suggests
that both contributed, because injection of anaesthetic into the
joint impaired performance when the muscles were disengaged
without abolishing d l awareness of movement (though this
residual sensitivity might perhaps have been due to incomplete
 joint anaesthesia). It should also be noted that cutaneous inputs
are important not only for any phasic information they provide
about movement, but also in setting the excitability of the
central sensory mechanisms. Clark et al. (1986) provided a
recent example of this Iatter effect by documenting the reduction
in the detectability of movements of the proximal interphalan-
geal joint of the index finger that can be produced by anaes-
thetizing the skin of the thumb.
Sense of absolute position
The above experiments were concerned essentially with the
detection of movement. Recent work by Clark et al. (1985,
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1986) strongly fortifies the case for the existence of a sense of
absolute position, distinct from any sense of movement, and
which seems likely to arise solely from muscle; the preferred
candidate for this must be the secondary ending of the muscle
spindle. What is normally called position sense would seem to
apply to a combination of sensations of movement and
sensations of position, which are normally inextricably inter-
twined. Clark et al. separated these by displacing a joint so
slowly that the subject was quite unaware of any movement
taking place. The slowest movements, applied to the ankle,
Can. J. Physiol. Pharmacol. 1988.66:430-438.
were 3.5" applied at 8.25"/min, and took nearly a quarter of an
hour to complete. The subject did not even have to pay attention
during this time, and at the end was asked how the angle of the
joint compared with the same one on the other side of the body,
or sometimes to locate by memory the initial position of the
ankle. The original experiments were on the knee. Here, as
elsewhere, they found that subjects were very good at recogniz-
ing a new position although they were quite unaware of any
antecedent movement; they just became aware that the angular
position had changed.
In recent experiments, on the ankle and on the metacarpo-
phalangeal joint of the index finger, Clark et al. (1985) studied
the effect of varying the velocity of displacement. They argued
that on lowering the velocity the performance of a sense of
absolute position would be relatively unaffected, whereas that
of a movement sense should be drastically disturbed. Under
normal conditions abduction at the metacarpophalangeal joint
elicited the response expected from a positional system, with
100% detection of 2.5" applied at all velocities. However, when
they eliminated the muscular contribution, while leaving the
cutaneous and joint contribution, the behaviour changed to that
of a velocity detection system and slow movements were not
perceived. This was done by anaesthetizing the ulnar nerve
which paralyses the relevant muscles while leaving the finger
itself unanaesthetized, since it is supplied by the median nerve.
Injection of local anaesthetic into the joint cavity had no effect
on normal performance, so there is no question of pure position
sense being solely due to joint afferents because animal
experiments show that these are then paralyzed. Broadly similar
results were obtained with the ankle; in addition, they determin-
ed the threshold of the least stimulus that could be detected,
whether as an absolute displacement or as a sensation of
movement. On reducing the velocity of rotation the threshold
first rose appreciably, but then settled at an approximately
constant vdue irrespective of further reduction in velocity.
It may be concluded from all this that muscle afferent input
can lead to a sense of absolute position independent of any sense
of movement. It must, at least partly, utilize its own peripheral
afferent machinery, most plausibly the secondary ending of the
rnuscle spindle. In addition, muscle afferents (probably from
the primary spindle endings) contribute to a sensation of joint
movement; for the fingers these are probably normally assisted
by cutaneous and joint affesents, perhaps as a special case.
There is a final complication with these otherwise relatively
straightforward conclusions. When Clark et al. (1986) went on
to study the proximal interphalangeal joint of the index finger, it
was found to lack an absolute position sense, while having a
normal movement sense, some of which must have been derived
from muscle. The adjacent metacarpophalangeal joint, how-
ever, does have pure position sense both for flexion and for
abduction. They pointed out that the two interphalangeal joints
of a given finger cannot be moved entirely independently, and
there may not be a unique relation between the lengths of the
various muscles involved and the angle of each sf the joints, so
the CNS might be faced with an insoluble set of equations in
determining the absolute position of both joints on the basis of
muscle afferent signals; but this does not entirely resolve the
puzzle. From ordinary introspection we would seem to be just as
aware where our fingers are, as we are for our other joints, so we
would seem to be synthesizing a similar subjective concept
(namely position) from a different type of neural operation,
since we do not actually have a measure of absolute position.
The peripheral neural machinery would seem likely to be equally
present for all muscles, with both primary and secondary
spindle afferents, but we do not seem to avail ourselves of this
information which, even if not entirely unique, would seem able
to contribute.
Problem of' decoding spindle messages
Accepting the evidence that muscle receptors are crucially
implicated in position sense leads inevitably to the question:
How easily can their messages be read? The answer is not at all
readily, and we have practically no information as to how it is
done. Indeed, some earlier workers were so appalled at the
complexity of the task that they simply refused to accept that
muscle receptors could be involved in position sense (for
example, Mountcastle and Powell 1959). Let me run through
some of the difficulties, most of which have recently been
emphasized by Burgess et al. ( 1982).
(1) The rate of firing of spindle receptors depends in a
complex manner on both the length of the muscle and the way in
which it is changing, and particularly whether it is lengthening
or shortening, so no one receptor gives us a simple measure of
any one physical variable. As already noted, one might perhaps
be able to do something about this by appropriately combining
information from both primary and secondary endings.
(2) The rate of firing when muscle length is held constant
varies both with the length of time the muscle has been held at
the new length (adaptation) and on whether the length was
reached by stretching or releasing the muscle. Such effects
might perhaps be less marked when the spindles are under their
normal fusimotor drive rather than being studied in de-
efferented preparations. In this respect it is interesting that
Paillard and Brouchon (1968) showed that the accuracy of
matching the position of one a m with that of the other was
better when the first a m was moved actively by the subject
rather than passively by the experimenter. In addition, they
found systematic distortions of position sense with the passage
of time from the initial movement and the subsequent matching,
so perhaps not all these receptor errors are fully corrected.
(3) Wei et al. (1986) emphasized that in the absence of
contraction the muscles acting across the cat ankle fall slack
when the joint is near one or other of its extremes and then no
longer change in length with small changes in the angular
 434 CAN. 4. PHYSIBL. PHARMACOL. VOL. 66, 1988
position of the ankle. Their spindles then cease to provide a
signal of joint movement while those in the now well-stretched
antagonist continue to do so, and the same seems likely to hold
for man. Thus, as already concluded from the effect of
vibration, human position sense must be compounded from both
agonist and antagonist signals.
(4) Simple hinge joints with a single degree of freedom are a
very particular case, and even here a given muscle may act at
more than one joint. Thus, and even more so with ball and
socket joints, the activity of receptors in different muscles must
be combined by means of appropriate algorithms to produce a
unitary position sense and spatial map of the body.
(5) More fundamentally, the familiar frequency code of
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afferent firing is employed to indicate position, that is,
topography, rather than to signal intensity; this contrasts
powerfully with the cutaneous system where we are used to
thinking of higher frequency firing as leading to a more intense
subjective sensation. This may perhaps be true also for
sensations of joint mvement; but, as emphasized by Burgess et
al. (1982), the quality of one's awareness of the absolute
position of a limb seems much the same throughout the normal
range, yet under static conditions the summed discharge of
spindle receptors seems likely to be much greater at the
Can. J. Physiol. Pharmacol. 1988.66:430-438.
extremes. It follows also that if the map of the body image is laid
out in some topographical manner across an m a y of nerve cells,
that is, as a spatial code, then the initial frequency code has to be
totally transmuted.
Fusimotor action and need for cors&&ary discharges
The need for neural processing of the raw receptor signals is
shown even m r e clearly on considering the effects of fusimotor
activity on the afferent discharge. Fusimotor input does two
separate things to the spindle afferents. First, it biases them so
they fire at a greater rate for a given muscle length. Second, it
changes their sensitivity to externally applied stimuli. In other
words, the spindle afferents have a variable calibration, so their
discharges cannot be interpreted in quantitative mechanical
terns of joint angle and so on without a knowledge of their
current sensitivity, since this may be varying from moment to
moment. In principle this is readily done by supplying the
reading centres with corollary discharges indicating the current
level of fusimotor activity, and hence the correct calibration
factor. The two separate systems of fusimotor fibres, the static
and the dynamic axons, seem to be able to change the static and
dynamic calibrations sf the endings relatively independently, so
making the appropriate adjustments is no mean task. It would
seem to be made yet more complex by the existence s f beta
axons that supply both the spindles and the extrafusal muscle
fibres.
Let us turn next to the problem of spindle bias, since this is
somewhat easier to think about. When a conscious human
subject makes an isometric contraction, his spindles fire faster
because the gamma efferents have been co-activated along with
the main alpha motor fibres. If this Ia discharge had k e n elicited
by stretching the muscle, the subject would have felt that the
appropriatejoint was rotating, but as is easily verified when one
es an isometric contraction against a table there is then no
experience of movement. Thus here is a ""sensory signal" that
fails to elicit a sensory experience. The likely reason is that the
afferent message is read in conjunction with a corollary
discharge from the motor centres signalling that the movement
has been commanded so that the consequential sensory excita-
tion can be discounted.
A complementary sbsemation was provided by Hulliger et al.
(1982) when they recorded the discharge of a human spindle
afferent from a contracting finger extensor while the subject was
moving his finger against a constant load from one position to
another; movement was restricted to the metacarpophalangeal
joint. They found that the spindle firing was the same whether
the muscle was long or short, indicating that the change in
fusimotor activity had precisely counteracted the normal length
sensitivity of the afferent. Yet the subject was aware that the
position of his finger was different. So here there seems to be a
sensory experience in the absence of the expected afferent signal
(the antagonists, however, were not studied). They were
obviously thoroughly puzzled by this and after briefly mention-
ing ways to escape from the conundrum finished by saying
"Thus, in spite of the absence of explicit position monitoring
some remote possibilities remain that muscle spindles may
provide central structures with infomation that might contri-
bute to position sense." But there is nothing remote about a
spindle contribution, once one accepts the inevitability of
corollary discharges contributing to the analysis. Rather, given
what we h o w about other systems, it is naive to suppose that
they are not involved and to treat a search for them with the
microelectrode as being rather like trying to find the soul.
Proven action of cgero%lary discharges in other systems
It seems pertinent to describe three sets of observations
testifying to the reality of corollary discharges.
Oculsrnotor system
First, there are those of Guthrie et al. (1983) which show that
the oculomotor saccade control system of a conscious monkey
continues to know the position of the eye in the orbit, quite
independently of visual clues, after deafferentation of the
extraocular muscles. This can then only come from c o r o l l q
discharges. Second, again from the oculomotor system, Rich-
mond and Wurz (1980) recorded from cells in the superior
colliculus, which responded quite differently to translation of
the visual image across the retina depending upon whether this
was done by the experimenter displacing the external visual
scene, or by the monkey itself making a saccadic eye move-
ment. This difference demanded that the coHicular cells
received signals related to eye movement as well as from the
retina. Because the essentials of such behaviour remained after
paralysing the eye muscles and preventing overt saccades,
corollary discharges are shown to have been involved.
Electric jsh
Third, turning to a quite different part of the animal kingdom,
there are Bell's (1982) striking findings on the momyrid
electric fish. This species both sends out its own electrical pulses
and, apparently quite independently, has specific ampullaq
electroreceptors to pick up external electrical fields preexisting
around itself. These external signals would, however, be
jammed by its own activity, so whenever the momyrid emits an
electric discharge it sends a corollary discharge to its receiving
centres to prevent this happening. Their action on neurones in
the sensory receiving centres can be directly observed with a
microelectrode. The situation is simplified by curarizing the Ash
so that no actual electrical discharge occurs. Instead, an
artificial discharge is produced by picking up the descending,
but now ineffective, motor volley to the electric organ with an
electrode in the tail, and then using this to trigger an electrical
stimulator acting through the water around the fish. This
 MATTHEWS
artificial electric input elicits a complex pattern of excitation and
inhibition from the appropriate central sensory neurone. On
commencing such stimulation there is initially no corollary
discharge to the newone, since it gives no response when there
is a descending motor command to the electric organ without an
actual electric discharge, whether real or artificial. However,
when the artificial discharge is regularly paired with the
"command" of the descending motor volley, then over a period
of 5 min a corollary discharge gradually develops and the
sensory neurone comes to alter its pattern of firing to the
command signal occurring on its own, without the superadded
electrical stimulus. The purely corollary-evoked response was
very approximately the mirror image of the direct response to
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stimulation, unmodified by a corollary. Moreover, the response
to the stimulus was appreciably reduced when the neurone was
simultaneously acted upon by the corollary. When the fish was
left undisturbed for 15 min or so the corollary seems to be
switched off, since the command motor discharge no longer
produces an effect on the sensory neurone. Recording from the
primary afferent fibres confirmed that their behaviour was
constant throughout, and that they were not under efferent
control.
Several lessons can be derived from all this. First, a signal can
Can. J. Physiol. Pharmacol. 1988.66:430-438.
occur in a sensory neurone on dispatch of a motor message; that
is, we are looking at the direct effect of a corollary discharge.
Second, the genesis of this corollary is highly plastic and in this
case it is only produced if the command elicits an unwanted
sensory input. Third, the pattern of the corollary is tailored to
the pattern of the unwanted input; this was demonstrated yet
more fully in other experiments in which the timing, polarity. or
size of the stimulus was varied. Hence this particular corollary
has some of the properties of the efference copy postulated
many years earlier by von Holst, which could be used to annul
the unwanted signal by simple subtraction. Fourth, one should
note that this electric fish has two other sets of electroreceptors
which are used for quite different purposes and for each of
which corollary discharges are also used centrally but in
different ways, with neither behaving like efference copies
(Zipser and Bennett 1976; Bell 1984). One system, which is
used to detect the discharges of other fish, is simply briefly shut
off by the corollary of the emitting fish. The other system, which
is used to detect the electrical effects of the fish's own pulses, is
briefly facilitated by the corollary. Thus corollary discharges
can be employed in several different ways and be of various
kinds. Finally, and most importantly, if this level of the animal
kingdom can produce and use corollary discharges of such
variety and sophistication, we have no right to have survived in
the evolutionary struggle if we cannot do as well.
Mode of action of coro llaries in proprioception
Returning to the main theme, the interest now is not in asking
simply whether corollary discharges are involved in the genesis
of human position sense, for it seems to me that they must be.
The current questions are where do they occur, and how are they
used? Here the only definite thing to say is that, as far as the
sense of movement is concerned, they do not behave like the
most elementary types of efferent copy and are not capable on
their own of initiating a sensory experience. This was empha-
sized by Goodwin et al. (1972) on the basis of their observations
of making one a m ischaemic by inflating a blood pressure cuff
around it and so pardysing both sensory and motor axons. Just
before paralysis is complete the subject passes through a stage in
which he can make finger movements without being aware that
435
he has done so, although of course he knows he has tried. Thus
there is the interesting situation that a subject can dispatch a
motor command, and presumably with it the normal corollary
discharges, and actually make a movement which the sensorium
entirely fails to register. Presumably, ischaemia paralyses
sensory axons slightly in advance of motor axons, thereby
removing the signal that the sensorium normally relies upon to
tell it what has happened, and the continuing corollary dis-
charges cannot take their place. It might be suggested that the
corollary discharges were indeed simple efference copies, but
were purely inhibitory discharges requiring subtraction from
excitatory signals and that in the absence of these, with afferent
paralysis, the system was just biased into total inactivity. But
this will not explain the similar finding obtained when the
subject is curarized, whether locally or generally (McCloskey
and Torda 1975; Stevens et al. 1976). Local paralysis can be
obtained by injecting curare into a vein when the circulation is
occluded, while total paralysis is a much more heroic proced-
ure. In both cases when the subject attempts to move, he has no
sensation of any movement occurring and indeed is acutely
aware that he is quite unable to move. Stevens (1978)
commented that with whole body paralysis "one felt like a solid
piece of cement. It was very much like being buried alive." In
this case, many spindle afferents should have been continuing to
fire tonically, in spite of being deprived of fusimotor drive, so
any inhibitory corollary discharges would have a background of
sensory activity to modify.
One might take this as evidence that corollaries don't exist,
but it seems much more likely that, in the late Donald MacKay's
tern, they are used to evaluate a sensory message rather than
simply suppress it. Thus to experience movement, there has to
be a change in afferent firing for one to be aware of anything
happening, but the responsible afferent signals have to be read
with the help of corollary discharges. However, it is not yet
clear whether this failure of corollary discharges to produce an
effect on their own applies equally to the sense of absolute
position, and more particularly for motor coordination involv-
ing spatial mapping. This has been emphasized by Stevens
(1978) on the basis of his own experiences of total extraocular
paralysis. On attempting to move his eyes he had the bizme
experience that though the visual world showed no sign of
movement, it was somehow displaced. This was not primarily a
visual experience, but seemed to have more to do with the
spatial mapping required for movement. When the paralysis
was produced by retmbulbar injections of anaesthetic, he
systematically missed on pointing at a target when he was trying
to look to one side. The analogous experiment of pointing to a
paralysed limb that one is trying to move has yet to be
performed. Thus the precise role of corollary discharges in the
synthesis of the body image remains an enigma, and some may
well continue to question their existence. In the related question
of the awareness of "heaviness," however, there is strong
evidence again that they take part, but can now, of themselves,
elicit a conscious percept (McCloskey 1981; Gandevia 1987).
Complications ingroduced BPg, tendon compliance
Further investigation requires one to remain continually alert
as to how the peripheral machinery behaves, for this underlies
all our sensory judgements, and unsuspected peripheral effects
may be lurking in the background ready to mislead. A particular
observation for which this might be so is the effect of a changing
level of contractile force in distorting perception of the extent of
a voluntary movement. Three separate groups of workers
 436 CAN. J. PHYSIBL. PHARMACOL. V O L . 66, 1988
(Roland 1978; Wymer and D' Almeida 1980;Watsonet al. 1984)
have independently described the phenomenon in apparent
ignorance of each other's contribution. It is that when one
makes a movement requiring an increasing strength sf contrac-
tion as one moves, as against a spring, then the extent of the
movement is systematically overestimated by an amount
increasing with the increase in exerted force. No such effect is
found when a constant force is exerted throughout the course of
the movement. Without finally deciding the matter, the various
authors seem to have felt that this should be attributed either to
an interaction between the signals from spindles with those from
tendon organs or more likely to an interaction with changing
corollary discharges.
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A mush more prosaic possibility, which is ripe for study, is
that the error is a simple consequence of the tendon stretching
under the increasing contractile force, SO that the muscle was
shorter than would otherwise have been expected from the overt
psition of the limb or digit. If so the production of an equivalent
muscle shortening at constant force, which provides the
standard of reference, would entail a greater joint movement,
since none of the muscle shortening would be lost in the tendon.
Rack (1985; Rack and Ross 1984) has recently emphasized how
greatly tendons may stretch under their normal loads and the
Can. J. Physiol. Pharmacol. 1988.66:430-438.
inescapable implications of this for motor control; for example,
the tendon of the long flexor of the human thumb may elongate
by an amount equivalent to a joint movement of 7O for an
increase of load from 8 to 25% maximal, and by a similar
amount again on increasing the contraction to maximal. It seems
inevitable that such simple mechanical behaviour must contrib-
ute to the observed psychophysical effects, but whether it could
be totally responsible remains to be tested. The moral to be
drawn is that there is no escape from continuing attention to the
peripheral machinery, even when one's chief interest is in
central mechanisms.
Central maps
Piasticity of body image
Finally, there are various recent psychophysical experiments
that illustrate the complexity of the central maps we have of our
body image and of their relation to the external world. Most of
them use vibration as a way of injecting an abnomal level of
proprioceptive input, presumably chiefly from the spindle
primary endings. First, Craske (1977) vibrated the wrist flexors
in the forearm and asked subjects to p i n t to where they felt their
wrist to be.As usual they indicated that they felt the joint to be in
the position it would be in if the flexors had been stretched, and
the wrist was felt to be extended. The new thing he stressed was
that the subjects were quite prepared to indicate that the wrist
was hyperextended far beyond its normal range of movement.
In other words, the map is highly labile and does not have built
into it a knowledge of what is anatomically possible. Using the
map is not like consulting a pre-existing atlas where one can
only find that which has already been charted. Rather one would
seem to be modifying the mapas one uses it, and letting current
observations override all previous experience. Another example
of this has very recently been provided by 9 . 8 . Lackner, as yet
unpublished. He vibrated the biceps while the subject was
holding onto his nose and who, as usual, felt that his elbow was
extending. But since the stationary nose was still being held this
produced a sensory conflict, arising from the contradictory
infomation as t s where his m was. Some subjects solved this
problem very simply and logically, but by entirely unconscious
nervous operations acting on their internal body map, and had
the clear subjective impression that their nose was growing out
and elongating so as to remain in contact with the apparently
moving m. As one said, "I feel like Pinocchio." So once again
the body map can be temporarily redrawn on the basis of a
fleeting sensory input.
J. R. Lacher has produced a large number of other
illustrations, similar in principje, on vibrating a variety of
muscles in subjects adopting a variety of postures. There was a
high degree of variability between different subjects as to how
their sensory analysing centres responded to this unusual chal-
lenge. But the abiding principle was that our subjective map sf
our body is fluid and highly modifiable from moment to
moment. It cannot consist simply of a Cartesian doll with its
joints movable over a known range. From the point of view of
the control of movement, however, one suspects that there must
be other maps with the anatomical constraints built in, since it
would be a disaster if we were to use our full muscular power to
try to drive our joints beyond the range they are designed for.
Perhaps the real job of the joint receptors is indeed to act as
"limit detectors," and to provide this information in a totally
unambiguous manner for the motor system, rather than to keep
our subjective sensory map updated. This woujd At well with the
gross pathological effects seen with denemation of joints.
Relation of body to externaH space
Next there is the use of vibration to alter one's subjective
experience of the location of objects in external space; this
demonstrates that there are powerful interactions between quite
different types of neural signal. In an experiment by Lackner
and Levine (1978; Levine and Lackner 19'79) the subject sat in
darkness with a light source attached to his hand and which he
fixated. The elbow flexors were vibrated, the a m was felt to
move, and with it the light appeared to move in space. The
abnormal proprioceptive input had taken precedence over the
normal cues of the orientation of one's eyes. In related
experiments the same sort of thing was found for a localized
auditory stimulus, suggesting that-it is not simply a matter of
preferring the measure of the length of one set of muscles (the
elbow Wexors) over that of another set (the extraocular muscles)
but rather a remapping of one" spatial orientation. Biguer et al.
(9986) applied vibration over the small muscles at the side of the
neck and so, presumably, causing their muscle spindles to send
the usual false signal of their length, thereby producing a false
indication of the orientation of the head on the body. Again,
small lights viewed in darkness were perceived as moving,
although the head and the eyes were still. Moreover, when the
subject attempted to point at them, he systematically missed
them. In this case there should have been no abnormality in the
signals from the muscles that were being used to move the a m .
Again, spindle input would seem to have led to a remapping of
space, both subjectively and for motor commands. All these
experiments establish that spindles provide information not only
for the creation of a subjective map of the body, but also for the
orientation of this map in the external world.
Increased gravity
It might be suggested that vibration is not quite to be trusted,
that not only is it generating an abnomaljy high spindle input,
but that it is also exciting a mass of extraneous jamming signals
from a variety of other phasically sensitive receptors, so that we
are witnessing a failure of the analysing centres rather than
getting a glimpse of how they nomdly handle spindle data.
Against this are the observations of Lackner and Graybiel
(1981, 1984) on some subjective effects of temporarily increas-
ing akne apparent force of gravity. This was done by diving a
large jet aircraft from 32 000 to 24 000 f ( 1 f = 8.385m) and
 then back up again along an appropriate trajectory. In the
pull-up phase the apparent gravitation force was held at 2 g as the
plane accelerated upwards. During this time the subject is told to
step on and off a low stool. Not surprisingly he finds the
stepping up requires unusually great effort; but, in addition and
quite unexpectedly, he has the illusion that the stool sinks down
as he steps onto it. This seems likely to arise because the normal
spindle pattern of firing has been changed as a result of
interference with the normal relation between the rate of
movement, and the amount of alpha motor discharge, and the
level of co-activated fusimotor activity. One may conclude,
without getting entangled in the details, that once again muscle
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a f f e ~ n activity
t is being used to alter one's perception of the
external world, as well as of one's own body image; cutaneous
afferent activity might equally be involved. The power of such
action was shown yet further when the subject did simple knee
bends, moving himself up and down during exposure to 2s. In
addition to experiencing movement of the floor beneath him, he
had the visual illusion that the whole plane was moving as well
as himself; when he went down it rose, when he stood up it
usually sank. It may again be concluded that somatic sensory
activity plays a part in the mapping of external as well as internal
Can. J. Physiol. Pharmacol. 1988.66:430-438.
space.
Mu ktiplicitg?of mops ?
k t me give you a final question: Is there just one map of our
body image which we use equally for sensory and for motor
purposes? The answer seems likely to be no. First, we have the
example of the visual system before us. As long known, patients
with damage to the occipital cortex are blind, in that they say
they cannot see; they have no consciously accessible visual map
of the external world. However, Weiskrantz et al. (1974)
showed that if a light is flashed in a variety of positions these
"blind" subjects can point rather accurately to its position, even
though they have not consciously seen it. Thus their motor
machinery still has access to a map of the external world which
has an input from the retina. This so-called "blindsight"
indicates the existence of a topographically organized map of
visual space lying outside the normal visual cortex, and beyond
the reach of our normal conscious self. The irrelevance of the
conscious map of visual space for another motor act, namely the
control of saccadic eye movements, was shown by Lackner and
Levine (1979) by distorting the conscious map by
The subject had a light attached to his hand which he perceived
as moving to a new position when biceps were vibrated.
However, when told to look at the light he made saccadic
movements to its true position rather than to its perceived
position; his eyes were initially directed either at another target
light or at his other arm whose location was being accurately
reported by his position sense. Thus the saccadic generator was
using an undistorted map of visual space, while the conscious
self was being deceived.
Next, there are two surprising recent observations with
vibration which suggest that we may have more than one map of
limb position (Sittig et al. 1985; Sittig 1986). In one experi-
ment, the subject is ask& to track a moving target light with his
arm while it is being vibrated. As usual he thinks he is
sucwssfu~lydoing this, although he is showing the standad
vibration-induced mismatch (he cannot, of course, see his am).
He is then told to move his rapidly so as to align it properly
with the target. This makes no sense to him, since he thinks he is
already doing so; none the less he makes a movement and brings
the m accurately to the target. This suggests that certain motor
acts may employ a quite different map of limb position from that
available to the sensorium. Moreover, this motor map would not
seem to be using information from the spindle primaries or else
it too would have been distorted. In another experiment the
subject is told to move his am,again as fast as possible, from an
initial position to a target, which of course he can do. The m is
then vibrated at the initial position so that its real position and its
perceived position come to differ; normally it tended to flex
under the action of the tonic vibration reflex but felt as if it had
not moved. When told to move rapidly to the target the subject
did so as successfully as before. Electromyographic recording
showed that the motor discharge differed in the two cases, so
there is no question of his achieving the correct target simply by
the mass-spring properties of the arm operating upon an
invariant motor discharge. Rather, he behaved as if his motor
machinery h e w the correct position of the a m even though his
sensorium did not. The provisional conclusion would seem to be
that we have one map of the body which is consciously
perceived, distorted by vibration, and perhaps used to control
slow movements, and another subconscious map which is not
affected by vibration and which can be used to programme a
ballistic movement.
Conclusions
M a t final conclusions can be drawn from the varied matters
that have been discussed above?
First, we do now have a fair idea of the origin of the peripheral
messages underlying position sense, with muscle spindle
afferents given pride of place.
Second, these signals are by no means easy to read and
probably need to be processed both in relation to each other, and
in conjunction with corollary discharges from the motor centres.
Third, the maps they feed into are not just maps sf the body
itself but also include its relation to the external environment.
Moreover, these maps have a surprising degree of fluidity to
them, in that when the proprioceptive input suggests it the
sensorium makes little attempt to maintain the normal body
shape.
Fourth, we must be prepared to find more than one site of
mapping, with the maps probably being used for different
purposes. There is nothing surprising about this as electrophys-
iologicd recordings disclose multiple representations of a given
input. For those who would study such processing with a
microelectrode, the difficulties ape formidable; but given the
example of the visual system, the achievement may be great.
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